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Application of Diatom-Based Indices for Monitoring Environmental Quality of Riverine Ecosystems: A Review R. Venkatachalapathy and P. Karthikeyan

Abstract Diatoms are a large and diverse group of single-celled algae. Diatom-based indices are increasingly becoming important tools for assessment of environmental conditions in aquatic systems. Diatoms have long been lauded for their use as powerful and reliable environmental indicators. The objective of this paper is to review and explain the application of diatoms in environmental studies of river aquatic system. Review of Diatom Research in India and abroad shows that the diatom study and its applications are at nascent stage when compared to their utilization in Australia, Canada, United States and Brazil. The occurrences of Diatoms in surface waters especially in major rivers of the world are yet to be recorded. However, the review of Diatom Research provides considerable scope and applications in understanding and monitoring of environments. From the analysis of diatoms in surface waters of India, we conclude that the diatom studies can be best used in environmental assessments of water-quality of ecosystem. Keywords Diatoms ecosystem

Environment

Monitoring

Management

Aquatic

1 Introduction Diatoms are single celled microscopic algae that posses ornamented cell wall composed of silica (SiO2). They inhabit all the aquatic environments and are found in great abundances and diversity. The shape, size and pattern of silica frustules form the basis for classification and identification of diatom taxa. Due to their rapid response to environmental changes (Karthick et al. 2008; Venkatachalapathy and

R. Venkatachalapathy (&) P. Karthikeyan Department of Geology, Periyar University, Salem 636 011, India e-mail: [email protected] © Springer International Publishing Switzerland 2015 Mu. Ramkumar et al. (eds.), Environmental Management of River Basin Ecosystems, Springer Earth System Sciences, DOI 10.1007/978-3-319-13425-3_28

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R. Venkatachalapathy and P. Karthikeyan

Karthikeyan 2012, 2014), deterioration of water quality especially from impacts such as nutrient enrichment, acidification and metal contamination, diatoms have been used widely for biomonitoring of aquatic ecosystems (Cholnoky 1968; Lowe 1974; Schoeman and Archibald 1984, 1985, 1987, 1988; Somers et al. 2000; Kelly and Whitton 1995a, b). According to Kelly (1998a, b), diatoms are one of the basic components of river bio-monitoring and assessment of ecological status of rivers. These authors have also established many diatom indices for water quality assessment of rivers and lakes. Recent studies have shown that the diatom based indices vary in their capacity to ionic composition and organic pollution in rivers (Gomez and Licursi 2001; Taylor et al. 2007). The strong correlations between diatoms and ionic concentration enable diatoms to be used to reconstruct past changes in lake water salinity driven by hydrologic and climatic change (Fritz et al. 1993, 1999; Blinn 1995). Diatom assemblages in rivers and streams can be analyzed by rigorous statistical techniques to establish their relationship to the environmental factors. The relative abundance of diatom species is used as the most valuable characteristics of diatom assemblages for bio-assessment of river health. River health can be assessed by using diatoms [Prygiel and Coste (1993) in France, Harding and Kelly (1999) in UK and Stevenson and Pan (1999) in the USA]. A diatom has shorter generation times than fish and macro-invertebrates and responds rapidly to environmental changes, thus provides scope as early warning indicators for both pollution increases and habitat restoration success. Cost of sampling and analysis are relatively low when compared to other organisms. Diatom samples can be collected easily for long periods of time for analysis. Thus, the study of diatoms has become an important element of monitoring and assessment programs in countries around the world. Undisturbed core sediments from ecosystems will provide habitat history of surface water bodies (Amoros and van Urk 1989; Cremer et al. 2004; Gell et al. 2005). Past conditions in streams and rivers can also be assessed utilizing museum collections of diatoms on macrophytes and fish (van Dam and Mertens 1993; Rosati et al. 2003; Yallop et al. 2006). Environmental changes in marine, brackish waters and estuaries can also be inferred by diatom studies, although the techniques and interpretations are more challenging than those used in freshwater lakes and rivers (John 1983; Snoeijs 1999). Artificial substrata are used for precise assessments in streams with highly variable habitat conditions and natural substrate unsuitable for sampling. The latter may be the case in deep, channelized or silty habitats. Benthic algal communities on artificial substrata are commonly different than those on natural substrata (Tuchman and Stevenson 1980). Suitable laboratory methods and field-sampling methods should be followed to minimize errors in assessments of water quality in surface water bodies. This paper reviews developments in the diatom studies over the past few decades with special emphasis on the application of diatom indices for monitoring the environmental quality of freshwater ecosystems.

Application of Diatom-Based Indices for Monitoring …

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2 Prerequisites for the Study of Diatoms 2.1 Extraction of Diatoms The attached microalgae, of which diatoms are a dominant component, can be collected by scraping natural substrates in streams. Stones (pebbles) and macrophytes are good sources of diatoms (Fig. 1). Floating filamentous algae or floating wood and plant materials are often full of loosely attached diatoms (Fig. 2). Diatoms grow attached to concrete substrates in urban drains. Epiphytic diatoms grow attached to macrophytes and large algae. Metaphyton includes diatoms loosely attached to algal mats and filamentous algae. Typically diatoms can be seen in the form of brown or black, slimy coatings on stones, submerged plants and mud. The colored coatings may be removed with a brush, ‘spoon’ or blunt scalpel from hard substrates and by squeezing or washing off from soft substrates like macrophytes and filamentous algae. Benthic diatoms may be collected by ‘scooping’ the top 3–5 cm of the sediment of a stream, with a vial, but this method disturbs and mixes the sediments (Fig. 3). An intact ‘core’ may be collected, by pushing an inverted open vial (with a small hole at the bottom), into the sediment and lifting it up. Using this method one can collect epipelon (growing on mud) and episammon (growing on sand) intact from a specific area. Motile species are common in mud samples. Tyagi (1985) collected water samples from various water bodies viz., lakes, ponds, wells and drains in and around Delhi and treated them with concentric HCl acid and the supernatant was discarded. It was followed by addition of concentric H2SO4 to remove the organic material present in the sample material. The supernatant was cooled and added with solid NaNO3. Bhatt et al. (2005) used a sharp-edged knife to

Fig. 1 Epilithic diatom samples collection in Cauvery River

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Fig. 2 Macrophytes diatom samples collection in Cauvery River

collect epilithic diatom samples by scraping the rocks and boulder surfaces and collected scraps of 3 mm2. The epilithic diatom samples obtained thus were cleaned with nitric acid and potassium dichromate. The samples were centrifuged at 10,000 rpm for 10–30 min and the supernatant was discarded. The pellets were washed twice with Isopropanol, Xylene and by distilled water for making permanent slides using Canada balsam. Venkatachalapathy and Karthikeyan (2014) collected epiphytic samples from the Cauvery River by brushing the undersurfaces and petioles of at least 20 plant leaves and roots. The collected materials were preserved in formaldehyde (4 %). For Polarizing microscopic analysis, a 10 ml epiphytic and Epilithic subsamples were extracted and cleaned using 30 % H2O2 and concentrated HNO3. Singh et al. (2010)


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Fig. 3 Benthic diatoms samples collection in Cauvery River

collected diatom samples using planktonic mesh net (pore size 40 μm) and preserved it in Lugol’s solution and treated it hot HCl and KMnO4 method. Kociolek and Karthick (2011) collected samples from floating aquatic plants at Kodaikanal Lake by scrubbing the plants with a toothbrush and the resultant suspension was preserved in ethanol. The samples were digested using concentrated nitric acid and centrifuged several times to remove the acid to prepare the diatom slides. A list of procedures involved in collection and segregation of diatoms are listed in the Table 1.

2.2 Preparation Diatom Slides Fresh samples should be examined, if habit and chloroplasts are to be observed. ‘Colonies’ are disintegrated by the processing employed for permanent preparation. Chloroplasts are destroyed by the chemical processing required for making permanent slides. If diatom samples are preserved by Lugol’s solution, 4 % formalin or Transeau’s Algal Preservative (6:3:1 = Water, Ethyl alcohol, Formalin), colonial structure and chloroplasts can be retained. Concentrated diatom samples are boiled in 50–60 % Nitric Acid to oxidize the organic materials and then the acid is washed off with deionizer water by settling or centrifugation. The final ‘cleared’ diatom samples-an ash colored material is mounted in a mounting medium e.g. Napthrax with a refractive index close to 1.7 and placed on a hotplate until the solvent in the medium evaporates. The slide is cooled immediately, by removing from the hotplate. The diatom slide thus obtained is permanent. The diatoms cleaned cells in permanent slides are observed under ×40 and photographed using black and white for best results or by digital photography.

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Table 1 Methods used by researchers for diatom slides preparation Author(s)

Material

Frederic Rimet (2012)

Epilithic

Methods

4 % formaldehyde. In laboratory, the diatom valves were cleaned using 40 % H2O2 and HCl. Clean valves were mounted in a resin (Naphrax©) Solak (2011) Epilithic Diatoms were collected by scraping 20 cm2 area stones. They were cleaned with acid (HNO3) and mounted on microscopie for observation with a magnification of ×1,000 Kociolek and Epiphytic Using concentrated nitric acid and Karthick centrifuged several times to remove (2011) the acid Nenad Epiphytic 2.5 % neutralized formaldehyde. The Jasprica et al. material was treated with 10 % HCl (2005) add 30 % H2O2. 2.5 % neutralized formaldehyde. 10 % HCl and distilled water. Using Naphrax as the mounting medium Potapova Epilithic Oxidizing organic material in samples (2003) with nitric acid in a laboratory microwave oven and mounting cleaned diatoms in Naphrax Jiunn-Tzong Epilithic Lugol’s iodine solution immediately Wu (2002) after collection and cleaned with acid (acetic acid: sulfuric acid = 9:1) in the laboratory. Washing with deionized water, Naphrax John (2000) Epiphytic, Lugol’s solution, 4 % formalin or Epilithic Transeau’s Algal (6:3:1 = Water, Ethyl alcohol, 50–60 % Nitric Acid, Napthrax Epilithic growing on stones; Epiphytic growing on macrophytes

Environment

Country

River

France

River

Turkey

Lake

India

Lake

Croatia

River

USA

River

Taiwan

River

Australia

2.3 Classification and Systematic Descriptions The Classification and systematic descriptions of diatoms has been almost exclusively based upon frustules characteristics i.e., shape, size, symmetry, structure and density of striae, nature of raphe, copulae and processes on the valves. The biological species concept based upon reproductive isolation is difficult to apply to diatoms (Round et al. 1990). Natural population of large number of a taxon should be studied incorporating as many characters as possible in delineating a species. The classification of Diatoms by Round et al. (1990) recognizes diatoms as a division of Bacillariophyta with three major classes as follows: (a) Coscinodiscophyceae-(Centric diatoms); (b) Fragilariophyceae-(Araphid-pennate diatoms) and


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(c) Bacillariophyceae-(Raphid-pennate diatoms). The International Journal of Diatom Research-the official journal of the International Society of Diatom Researchers follows this classification.

2.4 Diatom Studies in India Diatom research in India has a history of over 100 and 50 years (Ehrenberg 1854). Notable works on diatom taxonomy from this region includes the publications of Skvortzow (1935), Gonzalves and Gandhi (1952, 1953, 1954), Krishnamurthy (1954), Gandhi (1959a, 1966, 1970, 1998), Venkataraman (1957) and Sarode and Kamat (1984). Most of these works focused on the pennate diatoms, with less or almost no attention given to the centric forms. In a major contribution to diatom studies, Desikachary and Ranjitha Devi (1986), Desikachary (1988, 1989) illustrated and described many recent marine and fossils centric forms from the Indian Ocean in the “Atlas of the Diatoms”. Similarly Gandhi (1952, 1955, 1956a, b, 1957a, b, c, 1958b, c, 1959b, c, d, 1960a, b, c, 1961, 1962b, c) Gandhi et al. (1983a, b, c, 1986), Trivedi (1982), Jakher et al. (1990), Dadheech et al. (2000), Singh et al. (2006, 2010), Kumar et al. (2008, 2009), Tarar and Bodhke (1998), Bhagat (2002), Mishra and Mishra (2002), Mishra (2006), Patil and Kumawat (2007), Anand (1998) have studied various aquatic systems. Algal Data Base of Tamil Nadu Environmental Information System (ENVIS) Centre in http://tnenvis.nic.in/tnenvis_old/images/Algal_Database.pdf reported 668 taxa of freshwater algae from Tamil Nadu. Among them 346 green algae, 219 bluegreen algae, 60 diatoms, 32 charophytes and 9 freshwater red algae are listed in Table 7, pp. 85–105. The algae reported in that work were collected from temple tanks, ponds, beach pools, roadside puddles in and around Chennai (Desikachary 1959; Iyengar and Desikachary 1981) and a few places near Madurai (Desikachary 1959), Tanjore (Subramanian 2001) Virudachalam (Subramanian 2000) and Pollachi (Sankaran 1992, 2002, 2005a, b). The only comprehensive work on freshwater diatoms not only from the plains but also from several localities belonging to Kodaikanal and Ootacamund is that of Krishnamurthy (1954). Diatoms are used as bio-indicators to assess the water quality of Cauvery River in parts of Tamil Nadu, Yercaud lake, Shevaroys hills, Tamil Nadu and surface water bodies in Manipur State NE India (Venkatachalapathy and Karthikeyan 2014; Venkatachalapathy et al. 2014a, b).

2.5 Diatom Studies in Other Parts of the World In Australia, Schmid (1874–1959) reported occasional records of diatoms in Australia. Wood (1961a) and Wood et al. (1959) reported the occurrence of marine and inland diatoms in Australia. However, John (1983) presented the first systematic

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treatise with micrographs, descriptions and ecological information of 360 diatom taxa recovered from Swan River Estuary, Western Australia which includes both marine and freshwater species. Diatoms as tools for assessing health of rivers and streams in the south west of Western Australia were carried out by John (1998). Palaeoecological studies using diatoms to infer past environmental conditions were attempted by several workers (John 1993c; Gell 1997, 1998; McBride and Selkirk 1998). Importance of identification of diatoms by comparison of the modern or fossil diatom with descriptions and illustrations in floras for specific geographical areas or particular ecological systems has been emphasized by Battarbee et al. (2001b). Information on floras in an electronic format are increasingly becoming available that can be accessed either by CD-ROM (Kelly and Telford 2007) or through the internet (Battarbee et al. 2001a). Use of electronic monographs is an important contribution in the time of rapidly declining basic training and expertise on diatoms taxonomy (Stoermer 2001). Patrick and Reimer (1966, 1975) are the guides widely used in North America. Krammer and Lange-Bertalot (1986, 1988, 1991a, b) are German language guides to the central European flora.

2.6 Keywords on Diatom Studies With the wide acceptability of diatom studies in environmental monitoring, there has been a growth of terminologies associated with such studies. Important among them are provided herein for the benefit of the readers: acidity index, acidophilous species, acidophilous algae, diatom index, diatom indicator, diatom indices, pollution indicator, pollution sensitivity index, saprobic index, saprobity, saproby index, tropic diatom index (TDI), trophic indices, trophic state.

3 Diatom Indices for Water Quality Assessment There are many varieties of Diatom Indices for water quality assessment of surface water bodies (Table 2). They include, but not limited to, Generic Diatom Index or GDI (Coste and Ayphassorho 1991), the Specific Pollution Sensitivity Index (Indice de Polluosensibilite Specifique) or SPI (IPS) (Coste in Cemagref 1982), the Biological Diatom Index or BDI (Lenoir and Coste 1996), the Artois-Picardie Diatom Index or APDI (Prygiel et al. 1996), Sladeceks index or SLA (Sladecek 1986), the Eutrophication/Pollution Index or EPI (DellUomo 1996), Rotts Index or ROT (Rott 1991), Leclercq and Maquets Index or LMI (Leclercq and Maquet 1987), the Commission of Economical Community Index or CEC (Descy and Coste 1991), Schiefele and Schreiners index or SHE (Schiefele and Schreiner 1991), the Trophic Diatom Index or TDI (Kelly and Whitton 1995a) and the Watanabe index or WAT (Watanabe et al. 1986).


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Table 2 Biotic diatom indices Abbreviation

Full name

Reference

IPS SLAD DESCY L&M SHE WAT TDI EPI-D ROTT IDG CEE

Specific pollution sensitivity metric Sládeček’s pollution metric Descy’s pollution metric Leclercq and Maquet’s pollution metric Steinberg and Schiefele trophic metric Watanabe et al. pollution metric Trophic diatom metric Pollution metric based on diatoms Trophic metric Generic diatom metric Commission for economical community metric Biological diatom metric Indice Diatomique Artois Picardie Pampean diatom index (IDP)

Coste (1987) Sladecek (1986) Descy (1979) Leclercq and Maquet (1987) Steinberg and Schiefele (1988) Lecointe et al. (2003) Kelly and Whitton (1995b) DellUomo 1996) Rott et al. (1999) Lecointe et al. (2003) Descy and Coste (1991)

IBD IDAP IDP

Prygiel and Coste (1999) Lecointe et al. (2003) Gomez and Licursi (2001)

In the twentieth century, many biotic diatom indices were developed in Europe. These include, the trophic diatom index (TDI) by Kelly and Whitton (1995a) in Great Britain, the generic diatom index (GDI) by Rumeau and Coste (1988), the specific pollution-sensitivity index (SPI) by Cemagref (1982) and the biological diatom index (BDI) by Lenoir and Coste (1996) and Prygiel (2002) in France, the eutrophication pollution diatom index (EPI-D) by DellUomo (1996) in Italy, the Rott saprobic index (Rott et al. 1997) and the Rott trophic index (Rott et al. 1998) in Austria, the Schiefele and Kohmann trophic index by Schiefele and Kohmann (1993) in Germany and the CEE by Descy and Coste (1991) in France and Belgium. The diatom assemblage index of organic pollution (DAIPo) was developed in Japan (Watanabe et al. 1986) and the saprobic index (Pantle and Buck 1955) in the USA. These indices were later tested in neighboring regions. In Spain, Goma et al. (2004, 2005) and Blanco et al. (2008) tested the SPI, BDI, TDI and EPI-D in Cataluna, East Spain and north-West Spain respectively. Torrisi and DellUomo (2006) and Battegazzore et al. (2004) tested the EPI-D in Italian rivers and compared its performance with those of other diatom indices. In Germany, Koster and Hubener (2001) tested the Rott saprobic index, the Rott prophic index, the TDI, the Lange–Bertalot classes, the CEE index, and the Schiefele and Kohmann trophic index in German rivers. Kelly (2002) and Kelly et al. (2009a) tested the TDI for assessment of river quality in English rivers. Diatoms also enabled efficient assessment of the quality of Moroccan rivers (Fawzi et al. 2002). Several studies reported the use of diatom indices in regions with very different climates from the area they were created. Thus the TDI and GDI were tested in East Africa (Bellinger et al. 2006; Ndiritu et al. 2006) and the saprobic index and the TDI were tested in Malaysia (Maznah and Mansor 2002). The TDI was also tested in Australia (Newall and Walsh 2005), the Himalayas (Juttner et al. 2003) and Iran

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(Atazadeh et al. 2007). The GDI, SPI, BDI, and EPI-D were tested in South Africa (Walsh and Wepener 2009), the TDI and Rott saprobic index in Turkey (Gurbuz and Kivrak 2002; Kalyoncu et al. 2009a, b), and the SPI, BDI, and DAIPo in Vietnam (Duong et al. 2006, 2007). Dela-Cruz et al. (2006) tested the suitability of ecological tolerances/preferences of diatoms (Lange-Bertalot 1979) defined in the northern hemisphere in Australian rivers. In all cases, even if these diatom indices and diatom tolerances were developed and defined in very different regions (Europe, USA and Japan) from those where they were tested, pollution assessment results were good and demonstrated the robustness of diatom biomonitoring. In some cases diatom indices were applied in situations for which they were not planned: the SPI, GDI, BDI, and EPI-D were tested in springs and did not reflect their hydrochemical characteristics. When a field study is too different from the initially intended scope, the authors prefer to develop their own diatom index for their specific study. After testing European diatom indices, an Australian diatom index based on species determination was developed by Chessman et al. (2007). Eloranta and Soininen (2002) also tested an already existing trophic index, the TDI and proposed a new phosphorus diatom equation adapted to Finnish rivers. Lavoie et al. (2009) followed IDEC (Quebec diatom index) in Quebec Rivers, Canada and compared it with European and U.S. diatom indices. Lavoie et al. (2009) emphasized the importance of using diatom indices and suitable modifications to the regions of the study to obtain reliable results, especially for extreme conditions (very polluted or reference conditions). In South America, Lobo et al. (2004a, b) developed and integrated a biological water-quality index. Hurlimann and Niederhauser (2002) and Kupe et al. (2008) developed and tested a diatom index in Switzerland (DI-CH). In Taiwan, Wu (1999) developed and tested the generic diatom index (Wu and Kow 2002) whereas in China, Tang et al. (2006) developed their own multimetric diatom index and compared it with European diatom indices and confirmed that the Diatom indices are more suitable in assessment of river water quality. In U.S., Potapova and Charles (2003) developed and tested the U.S. diatom metrics for assessment of pollution in rivers. They have also compared the assessment of U.S. river quality with that of diatom metrics developed in Europe. Wang et al. (2005) developed a diatom index of biological integrity based on seven metrics for a particular U.S. ecoregion (interior plateau ecoregion). In India, Venkatachalapathy and Karthikeyan (2014) used many diatom indices for testing the water quality conditions of the Cauvery River. Based on the results obtained these authors have suggested that the diatom indices can be utilized for water quality assessment of Indian rivers. Thus, there is a consensus among the workers that the distribution of diatoms can be reliable indicators of ecological conditions of water (Cholnoky 1968; Lowe 1974) (Tables 3 and 4).


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Table 3 Class limit values for diatom indices. Eloranta and Soininen (2002) Index score

Class

Trophy

>17 15–17 12–15 9–12